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How can alien species inventories and interception data
help us prevent insect invasions ?
Marc Kenis, Wolfgang Rabitsch, Marie-Anne Auger-Rozenberg, Alain Roques
To cite this version:
Editorial Manager(tm) for Bulletin of Entomological Research Manuscript Draft
Manuscript Number: BER-06-158R1
Title: How can alien species inventories and interception data help us prevent insect invasions? Article Type: Full research paper
Keywords: invasive alien species; non-indigenous insects; pathways of introduction; economic impact; environmental impact; origin of alien species; feeding niche of alien species
Corresponding Author: Dr. Marc Kenis, Ph.D.
Corresponding Author's Institution: CABI Switzerland Centre First Author: Marc Kenis
1
How can alien species inventories and interception data help us prevent insect
2invasions?
34 5
Marc Kenis1, Wolfgang Rabitsch2,3, Marie-Anne Auger-Rozenberg4 and Alain Roques4 6
7
1CABI Bioscience Centre, 1, Rue des Grillons, 2800 Delémont, Switzerland. 8
2Austrian Federal Environment Agency Ltd. Dept. of Nature Conservation, Spittelauer Lände 9
5, 1090 Vienna, Austria. 10
3Institute of Zoology, University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria 11
4Institut National de la Recherche Agronomique (INRA), Station de Zoologie Forestière, Av. 12
de la pomme de pine, BP 20619, 45166 Olivet, France. 13 14 15 16 Correspondence author: 17
Marc Kenis, CABI Bioscience Switzerland Centre, 1, Rue des Grillons, 2800 Delémont, 18
Switzerland, m.kenis@cabi.org. 19
20
Abstract 1
2
Information relevant to invasion processes and invasive alien insect species 3
management in Central Europe was extracted from two databases: a compilation of two 4
inventories of alien insects in Austria and Switzerland, and a list of interceptions of non-5
indigenous plant pests in Europe gathered by the European and Mediterranean Plant 6
Protection Organisation (EPPO) for the period 1995-2004. For one third of the insects 7
established in Switzerland and Austria, the region of origin is unclear. Others come mainly 8
from North America, Asia and the Mediterranean region. Among the intercepted insects, 40% 9
were associated with commodities from Asia, 32% from Europe and only 2% from North 10
America. Sternorrhyncha, Coleoptera and Psocoptera were particularly well represented in the 11
alien fauna compared to the native fauna. In the interception database, Sternorrhyncha were 12
also well represented but Diptera accounted for the highest number of records. Sap feeders 13
and detritivores were the dominant feeding niches in the alien insect fauna. In contrast, 14
external defoliators, stem borers, gall makers, root feeders, predators and parasitoids were 15
underrepresented. Nearly 40% of the alien insects in Switzerland and Austria live only 16
indoors. Another 15% live outdoors but exclusively or predominantly on exotic plants. Less 17
than 20% are found mainly in “natural” environments. The majority of introductions of alien 18
insects in Europe are associated with the international trade in ornamental plants. An 19
economic impact was found for 40% of the alien insects in Switzerland and Austria whereas 20
none is known to have an ecological impact. The implications of these observations for 21
further studies and the management of alien species in Europe are discussed. 22
Keywords: invasive alien species; non-indigenous insects; pathways of introduction; 1
economic impact; environmental impact; origin of alien species; feeding niche of alien 2 species 3 4 5 Introduction 6 7
Invasive alien species are recognized as one of the leading threats to biodiversity. The 8
ways in which non-native species affect native species and ecosystems are numerous and 9
usually irreversible (Parker et al., 1999). Non indigenous species also impose enormous costs 10
on agriculture, forestry and human health (Pimentel et al., 2002b). Rapidly accelerating 11
human trade, tourism, transport and travel over the past century have dramatically enhanced 12
the spread of invasive species, allowing them to surmount geographic barriers. Since this 13
tendency is likely to increase (Levine & D’Antonio, 2003), national and international 14
strategies are required to assess the full scope of the threat of invasive alien species, and deal 15
with it effectively. 16
Insects represent the majority of living organisms and hence form a large part of the 17
alien species problem. In many regions, such as North America, Australasia and South Africa, 18
exotic insect pests are considered as important as native pests, if not more so (Pimentel, 19
2002b). Traditionally, problems have been less severe in Europe (Niemelä & Mattson, 1996). 20
However, in recent years several pests of economic importance have invaded Europe, 21
inducing more interest in the issue of alien insects. For example, the western corn rootworm, 22
Diabrotica virgifera virgifera LeConte is seriously threatening European maize production
23
and Dimic an insect of unknown origin, is causing much public concern because of its 1
spectacular damage on urban trees in Central Europe (Freise & Heitland, 2004). 2
Management of alien species invasion requires a good knowledge of invasion 3
processes, i.e. pathways of introduction, establishment processes, species traits and habitat 4
characteristics that favour invasion (Williamson, 1996; Wittenberg & Cock, 2001). It also 5
requires a precise assessment of economic and ecological hazards caused by the alien species 6
in order to improve risk assessments, define tolerance thresholds and evaluate the benefits of 7
control measures to be weighted against costs of control (Parker et al., 1999). Invasion 8
processes in invertebrates and pathogens are rather different from those observed in other 9
invasive organisms such as plants and vertebrates and, thus, require different strategies and 10
research priorities. Firstly, the introduction of invertebrates is usually accidental, biological 11
control agents being an exception (Causton et al., 2006). The introduction phase is rarely 12
observed and pathways of introduction are poorly known (National Research Council, 2002). 13
Secondly, when established in a new region, an insect quickly spreads to invade new regions 14
and habitats. In general, there is no obvious “lag phase”, as is often seen in plant invasions 15
(e.g. Lonsdale, 1993) and when a lag phase is observed, it is usually of short duration 16
(Memmott et al., 2005; Drake & Lodge, 2006). Consequently, an alien insect is usually 17
discovered when it is already firmly established, spreading and causing damage. An invasion 18
process is usually studied a posteriori, and management methods focus on the control of 19
already invasive, or damaging populations whereas, ideally, management efforts should be 20
directed to the first stages of the invasion processes by preventing introduction or develop 21
early eradication programmes (Puth & Post, 2005). 22
Nevertheless, a posteriori studies of already established alien insects are useful to 23
assess which taxonomic or bioecological groups of alien species are better invaders or more 24
(Mondor et al., 2006). Pathways and vectors of introduction can often be guessed from the 1
biology of the insect, supported by interception data from national phytosanitary services. 2
Such information allows the development or improvement of invasion risk assessment 3
methods for species, ecosystems or pathways (Wittenberg & Cock, 2002). 4
Some European countries have recently established national lists of non-indigenous 5
organisms, including insects, as part of a national strategy to address invasive alien species 6
(e.g., Essl & Rabitsch, 2002, for Austria; Geiter et al., 2002, for Germany; Wittenberg, 2005, 7
for Switzerland; Šefrová & Laštůvka, 2005, for the Czech Republic; Hill et al., 2005, for 8
UK). The objectives of the present study were to extract, from a combination of the Swiss and 9
Austrian lists, information relevant to invasion processes and invasive alien species 10
management in Central Europe. In particular, we assessed insect species traits that correlate 11
with the ability to invade and determined which habitats have been particularly susceptible to 12
invasion. We also identified the most likely pathways or vectors for insect introductions and 13
compared the results with a dataset of interceptions of non-indigenous insects in Europe, 14
collected by national services of inspection and quarantine. Finally, we evaluated the actual 15
and potential economic and environmental hazards linked to insect invasions in Central 16
Europe, and propose recommendations for management and conservation. 17
18
Material and Methods 19
20
Datasets
21 22
A dataset of 341 non-indigenous insects of Austria and Switzerland has been built, 23
based on recent lists for Austria (Essl & Rabitsch, 2002) and Switzerland (Kenis, 2005). The 24
(Kenis, 2005), i.e. (1) it is believed to be non-indigenous in Austria and Switzerland; (2) there 1
is proof or at least a high probability that the insect has been introduced into Europe by 2
human activities (or into Austria and Switzerland for insects of European origin); (3) it is 3
permanently established in Austria and Switzerland, i.e. it is self-reproducing and would 4
maintain populations even without new introductions; this includes also insects that survive 5
only in heated environments such as houses, stores, greenhouses, compost heaps, etc. The 6
Austrian list (Essl & Rabitsch, 2002) also includes non-established species and, thus, only the 7
insects that match the criteria mentioned above were incorporated in our dataset. 8
Archaeozoans, originally included in the Swiss list but not in the Austrian list, were included 9
in our analyses. A few non-indigenous insects have been added to the Austrian list since its 10
publication and data for some groups not treated therein (e.g. Diptera, Psocoptera, Anoplura) 11
were added from Fauna Europaea (2005). 12
Another dataset was built from data on the interceptions of non-indigenous plant pest 13
insects in Europe made by the national services of inspection and quarantine for the period 14
1995- 2004. These data were regularly reported as notifications of non-compliance (detection 15
of regulated pests) by the European and Mediterranean Plant Protection Organisation (EPPO), 16
and were recently synthesized by two of the authors (Roques & Auger-Rozenberg, 2006). It 17
does not include all insects intercepted but focuses primarily on alien insects that are on the 18
quarantine list of the EPPO or on insect groups that are potentially dangerous for plant health. 19
This database contains 6,743 interceptions of non-indigenous insects, from 28 European 20
countries, involving 13,558 individual specimens and 285 species identified to the species 21
level, of which 255 can be considered non-European. A sizable amount of intercepted alien 22
insects where identified at genus or family level only. From these, 19 genera were added to 23
thus, these genera represent additional species. Hence, the list of intercepted insects comprises 1
a total of 274 species. 2
To test the hypothesis that the taxonomic distribution of the non-indigenous insect 3
fauna in Switzerland and Austria is similar to the native European fauna, we used Fauna 4
Europaea (2005) as reference for the insect fauna in Europe. To test the hypothesis that the 5
taxonomic distribution of the non-indigenous insect fauna of North America origin in 6
Switzerland and Austria is similar to the native North-American fauna, we used Simberloff 7
(1986). 8
9
Area of origin of the insects
10 11
The area of origin of each alien insect established in Austria or Switzerland was 12
classified in one of the following regions: North America; Central and South America; Asia 13
(except Mediterranean area, but including Continental Asian Turkey); Africa (except 14
Mediterranean area); Eastern Europe; Southern Europe and Mediterranean region (including 15
Northern Africa and Middle East); Pacific region (Australia, New Zealand and other Pacific 16
islands); unknown. When the insect was thought to originate from two of these regions, the 17
closest region to Central Europe was chosen. A similar classification was used for the 18
interception data, but the origin was that of the commodity on which the insect was found 19
rather than that of the origin of the species. 20
21
Feeding niche
22 23
Each insect of the dataset was categorized into one of the following feeding niches: 24
casebearers; wood borers; root borers/feeders; seed borers/feeders; stem borers (including 1
twigs, buds and flowerhead borers); fruit borers; parasitoids; predators; ectoparasites; 2
detritivores (including saprophages, coprophages and mycetophages); omnivores. Insects in 3
which larvae and adults occupy a different feeding niche were classified by the feeding niche 4
of the larval stage. When the larva passes through two feeding niches, we chose the feeding 5
niche in which it spends the longest time. Insects for which the biology is not known were 6
assigned to the “most-likely” feeding niche, i.e. that occupied by taxonomically closely-7
related species. 8
An identical feeding niche classification was built for the European insects listed in 9
Fauna Europaea (2005), which comprises about 93,000 insect species. In this case, the 10
approximate proportion of each feeding niche was estimated by assigning each insect of the 11
list to the feeding niche encountered in its family or sub-family. For species-rich families and 12
sub-families showing two or more feeding niches, an approximate proportion of each feeding 13
niche was used, based on proportions calculated from regional or national checklists (e.g., for 14
diverse Coleoptera families and sub-families, we used Freude, et al., 1965-1983). We then 15
tested the hypothesis that the proportion of the feeding niches in the non-indigenous insect 16
fauna is similar to that of the native fauna. 17
18
Environment, host plant and EUNIS habitat
19 20
The following types of environments and host plants were used to classify the insects: 21
stored products (including non-food products such as fabrics, but not wood products); 22
domestic (i.e. living only in heated buildings, but not on stored products and not on living 23
plants in greenhouses); greenhouses; outdoors on indigenous host plant; outdoors on non-24
ectoparasite on vertebrates. Predators and parasitoids were categorized into the environment 1
of their main prey/hosts. Insects living in different environments were classified in the one 2
where they are most commonly found in Austria and Switzerland. Insects that are found 3
frequently on both indigenous and exotic plants were classified in the category “indigenous 4
host plant”. 5
In addition, each insect was categorized into one of the major habitat classes of the 6
EUNIS classification (EEA 2005) present in Austria and Switzerland: C, inland surface 7
waters; D, mires bogs and fens; E, grasslands and lands dominated by forbs, mosses or 8
lichens; F, heathland, scrub and tundra; G, woodland, forest and other wooded land; H, inland 9
unvegetated or sparsely vegetated habitats; I, regularly or recently cultivated agricultural, 10
horticultural and domestic habitats; J, constructed, industrial and other artificial habitats. 11
When an insect is known to occur in two or more habitat classes, the habitat in which it has 12
been most frequently reported was chosen. 13
14
Pathways and vectors of introduction
15 16
For each insect a pathway or vector of introduction into Europe (for non-European 17
insects) or into Austria or Switzerland (for European insects) was allocated. Since, in most 18
cases, the exact pathway is not known, the most likely vector was deduced by considering 19
their preferred habitats, life style or food plant. The categories used were: host plant; wood 20
material; stored products; biological control agents; host animal; others; multiple/unknown. 21
Insects with two or more possible pathways or vectors were categorized as 22
“multiple/unknown pathway”. The proportion of these estimated pathways and vectors was 23
compared with those of the interception dataset. The commodities associated with 24
bonsai trees, cut flowers, plants for planting, seeds), plant products for consumption (fruits, 1
stored products, vegetables), and wood and its derivates (wood, bark, wood packing material). 2
3
Economic and ecological impacts
4 5
An insect was categorized as having an economic impact when we found at least one 6
web page from Austrian, Switzerland or a neighbouring country describing damage and 7
suggesting control methods. Similarly, an insect was considered as having an ecological 8
impact when a publication or a web page from the same geographic region was found 9
describing an environmental hazard associated with this insect. 10
11
Results and Discussion 12
13
Comparison Between the Austrian and the Swiss databases
14 15
Despite their proximity and similarity in size, geography, climate, environment and 16
number of international ports of entry Switzerland and Austria have rather different alien 17
insect faunas. Of the 341 species of the combined database, approximately one third of the 18
species (35%) are known only for Switzerland (90 species) or only for Austria (30 species). A 19
significant proportion of species are recent invaders and their presence in the other country is 20
expected for the near future. Table 1 shows a selection of alien insects that are presently 21
recorded from one of the two countries only. Another factor that may explain the variation 22
between the two countries is the difference in taxonomic expertise in the two countries. Some 23
groups are better known in Switzerland (e.g. Diptera, Psocoptera, Sternorrhyncha), whereas 24
1
Origin of alien insects in Switzerland and Austria
2 3
For nearly one third of the alien insects in Austria and Switzerland, the region of 4
origin is unclear. In some cases, such as the horse-chestnut leaf miner Cameraria ohridella, 5
the insect appeared in Europe without having been described elsewhere and only data on its 6
population ecology, parasitism and dispersal biology lead to the conclusion that it probably 7
originated from another continent (Kenis et al., 2005). However, most insects classified as of 8
“unknown origin” are species whose distribution is cosmopolitan and for which there is no 9
agreement regarding their area of origin. This is particularly the case for the numerous stored 10
product pests and some ectoparasites on animal pets that presently occur on most continents. 11
The majority of the alien insects for which the area of origin is known came from Asia 12
and North America (Fig. 1), two continents that include regions climatically and ecologically 13
similar to Central Europe. A sizeable number of alien insects came from the Mediterranean 14
region, probably on their host plants imported to Central Europe as crop planting material or 15
products or as ornamentals. In recent years, Southern European species, e.g. moths and 16
dragonflies, have been increasingly observed in Austria and Switzerland. Many of them are 17
thought to migrate naturally, probably because of global warming, and are thus not included 18
in the list (Kenis, 2005). 19
Among the alien insects intercepted by European phytosanitary services, many were 20
found on commodities from Asia (39.8%) and other European regions (32.0%). Surprisingly 21
few were found on commodities from North America (2.3%) (Fig. 2), although North 22
American insects account for 18% of the alien insect fauna in Switzerland and Austria (Fig. 23
1). This discrepancy between interception data and the origin of established insects may be 24
numbers of North American species and individuals to establish more easily in Europe than 1
tropical species. In addition, the interception data being based on recent records only (1995-2
2004), the apparent difference with the alien fauna dataset may also reflect changes in foreign 3
trade in recent years, increasing exchange being made with more “exotic” regions, 4
particularly Asia for ornamental plants. Since the interception data concerned nearly 5
exclusively plant pests, it is not surprising to find many interception records on Asian 6
commodities. In their analysis of alien plant pests established in Great Britain, Smith et al. 7
(2005) also noted that Asia supplied a relatively high number of recent introductions. 8
Similarly, Haack (2001, 2006) noted that the most recent establishments and interceptions of 9
bark- and wood-boring Coleoptera in North America were or Asian origin. Furthermore, it 10
cannot be ruled out that the low occurrence of insects in North American imports may be due 11
to better sanitary practices in North America than in other regions. 12
13
Taxonomic Groups
14 15
Fig. 3 shows the taxonomic composition of the alien insects in Austria and 16
Switzerland, which significantly differs from the composition of the native insect fauna in 17
Europe (goodness of fit 2 test; 2 = 568.50; P<0.001; the 12 smallest orders of Fig. 3 being 18
pooled together to avoid low expected frequencies). Three insect orders and sub-orders are 19
particularly overrepresented in the alien fauna compared to the native fauna: Coleoptera, 20
Sternorrhyncha and Psocoptera. In contrast, Diptera and Hymenoptera are underrepresented. 21
A comparison between the alien insects of North American origin in Switzerland and Austria 22
and the native insect fauna in North America shows the same pattern (goodness of fit 2 test; 23
2 = 111.69; P<0.001; the 12 smallest orders of Fig. 4 being pooled together to avoid low 24
invading Europe than other insect groups (Fig. 4). Alien insects in the USA show the same 1
pattern, except that alien Hymenoptera are proportionally much more abundant in North 2
America, partly because of the large number of exotic parasitoids introduced into North 3
America for biological control purposes (Simberloff 1986). Nevertheless, there are also much 4
more alien herbivorous Hymenoptera, particularly sawflies, in North America than in Europe 5
(Mattson et al., 1994) This overrepresentation of Coleoptera and Sternorrhyncha may be 6
explained by the fact that beetles are easily transported in or with stored products whereas 7
aphids, scale insects and whiteflies are often carried inconspicuously with their host plant. 8
The interception data show a somewhat different pattern (Fig. 5). Sternorrhyncha were 9
also frequently intercepted but, surprisingly, Diptera accounted for the highest number of 10
interceptions. Two third of these were agromyzid leaf miners and the remaining one third 11
were mainly fruit flies of the family Tephritidae. However, the number of species intercepted 12
per order led to a larger representation of Sternorrhyncha and Coleoptera, whose respective 13
proportions were similar to those observed in the established alien fauna. Moreover, 14
interception data are strongly biased by the fact that surveys concentrate on plant pests. For 15
example, Hymenoptera, the vast majority of which are parasitoids, predators or nectar/pollen 16
feeders, are hardly represented in the interception data. Nevertheless, many plant pests 17
intercepted by phytosanitary services probably contained hymenopteran parasitoids that have 18
the potential to become established and invasive. 19
20
Feeding niche
21 22
The proportion of feeding niches in the alien fauna is significantly different from that 23
of the European fauna (goodness of fit 2 test, 2 = 366.57; P<0.001). Sap feeders and 24
Switzerland. Their proportion in the alien fauna is much higher than in the European fauna 1
(Fig. 6). The majority of the sap feeders are Sternorrhyncha, followed by other Hemiptera and 2
Thysanoptera. Small sap feeders are unnoticeably carried from one region to another attached 3
to seedlings, cut flowers, vegetables, etc. Detritivores are well represented in the alien list 4
because many stored product pests belong to this category. Other guilds that are 5
proportionally more represented in the alien fauna than in the European fauna are wood 6
borers, fruit borers, seed feeders/borers and omnivores. In contrast, external defoliators, root 7
feeders/borers, stem borers, gall makers, predators and parasitoids seem to travel or establish 8
less successfully. The number of parasitoids is most probably underestimated in our dataset. 9
The frequency of parasitoids in insect faunas varies from 8.5% to 25% according to different 10
estimations (Godfray, 1994). Hence, in Austria and Switzerland only 11 alien parasitoid 11
species (3% of the dataset) are recorded as probably established. All were released in Europe 12
as biological control agents. The absence of naturally introduced and established parasitoids 13
may suggest that these insects do not establish new populations easily. However, it almost 14
certainly also reflects their cryptic life-history and the taxonomic difficulties related to this 15
group. New indigenous parasitoid species are still described every year in Europe. Many 16
species are recorded from two or more continents, and it is probable that several of these 17
species invaded Europe from Asia or North America recently. 18
19
Environment, host plant and EUNIS habitat
20 21
Fig. 7 shows that nearly 40% of the alien insects in Austria and Switzerland live only 22
indoors, in houses, stores, greenhouses, etc. Another 15% live outdoors but exclusively or 23
predominantly on exotic plants. Following the EUNIS classification, less than 20% of the 24
recently cultivated agricultural, horticultural and domestic habitats, or in constructed, 1
industrial and other artificial habitats (Fig. 8). Among those insects that occur in “natural 2
environments”, the vast majority are found in forest habitats, which includes plantations. It is 3
a common observation that simple, disturbed, human habitats are more readily invaded by 4
insects and other invaders than complex, undisturbed, natural habitats. Elton (1958) attributes 5
this phenomenon to the “biotic resistance”, i.e. natural enemies and competitors that are more 6
prevalent in natural habitat than in disturbed habitats. Simberloff (1986) suggests two other, 7
more simple hypotheses to which we adhere. Firstly, disturbed, man-made habitats (i.e 8
agricultural and domestic habitats) are more important to humans and, thus, are studied more 9
carefully than natural habitats. As a result, new establishments are more likely to be detected. 10
Secondly, insects linked to human environments and activities (e.g. pests) are more likely to 11
be carried by human transports into a new region than insects living in natural areas. The 12
second hypothesis is confirmed by interception data that invariably contain far more 13
agricultural and domestic pests than insects linked exclusively to natural habitats. The first 14
hypothesis should be tested by extensive and specific surveys for alien species in natural 15
habitats. 16
17
Pathways and vectors of introduction
18 19
Among the 341 alien insects established in Austria and Switzerland, the exact pathway 20
of introduction is known with confidence for only the 12 biological control agents 21
deliberately released in Europe. However, for nearly 80% of the alien insect species, a likely 22
vector, usually a commodity, could be deduced or assumed based on their biology, plant or 23
animal host, etc. (Fig. 9). The main vectors of introduction were, in decreasing order, host 24
material. Of those insects that were probably introduced with their host plant (wood 1
excluded), at least 40% undoubtedly came on ornamentals and 20% on vegetables and fruits. 2
From insects assumed to have arrived with wood material, about two-third are associated with 3
wood (logs, processed lumber or fresh wood packaging) and one-third with old wood material 4
(e.g. furniture). The relative proportion of vectors assessed from the establishment data and 5
the importance of the ornamental plant trade as pathway is confirmed by the interception data 6
(Table 2). Cut flowers, seedlings (nearly exclusively for ornamental purpose), bonsai trees, 7
seeds and aquarium plants represented 52.7% of the commodities on which insects were 8
intercepted. Nearly 30% of the insects were intercepted on cut flowers, which is about the 9
same proportion found on fresh food (vegetables and fruits). The relative efforts put on 10
inspection of these different commodities is not known, however, considering that food trade 11
is far more extensive than ornamental trade, one can assume that proportionally much more 12
alien insects were found on ornamentals than on vegetables and fruits. Interestingly, more 13
insects were intercepted on wood packaging (4.3%) and bonsai trees (4.2%) than on logs, 14
processed lumber and bark (2.8%) (2 = 22.08, p < 0.01 and 2 = 19.40, p < 0.001, 15
respectively). The origin of the commodity on which insects were intercepted strongly varies 16
with the type of commodity. Asia seems to be the major source for insects on bonsai trees 17
(96.7%) and wood packaging (76.9%) whereas 47.9% of the insects intercepted on fresh 18
wood and bark came from Russia. 19
20
Economic and ecological impact
21 22
For 124 alien insects established in Austria or Switzerland (40% of all species) data on 23
economic damage are available from Austria, Switzerland or a neighbouring country. In 24
much lower than 5% (our estimates derived from numbers given in Pimentel, 2002; Pimentel 1
et al. 2002a; 2002b). Although alien insects represent only about 1% of the insect fauna in
2
Austria (Rabitsch & Essl, 2006) and 1.7% in continental United States (Simberloff, 1986), it 3
is usually estimated that between 30 and 45% of the insect pests in agriculture and forestry 4
worldwide are of alien origin (Pimentel et al., 2002a; 2002b).The higher rate of pest species 5
among non-indigenous faunas compared to indigenous faunas may be explained by three 6
factors that are not mutually exclusive. Firstly, alien insects causing economic damage are 7
more likely and more rapidly discovered than insects that are economically harmless. Thus, it 8
is very likely that many alien insects established in Austria or Switzerland in natural habitats 9
are yet to be discovered (Kenis, 2005). Secondly, insects are more likely to become pests as 10
introduced aliens than in their region of origin. Many alien insects having economic impact 11
are in fact of little, or of no importance in their region of origin, where they are controlled by 12
natural enemies and host resistance derived from co-evolutionary history (e.g. Löhr et al., 13
1990; McClure & Cheah, 1999). Thirdly, pests are more likely to invade new areas because 14
they are more abundant, their habitats are increasing in size and connectivity and they feed on 15
economically important plants or goods (Kenis, 2005). This is particularly the case with 16
stored product insects that have become pests in many regions and are regularly transported 17
with the commodities in which they live. 18
To our knowledge, no study has been carried out to investigate the ecological impact 19
of alien insect species in Austria and Switzerland, and only limited data are available for 20
Europe in general. A few alien insect species present Austria or Switzerland cause ecological 21
concerns in other regions. The ladybird Harmonia axyridis (Pallas), originally from eastern 22
Asia, is believed to out-compete and displace native aphidophagous species by predation and 23
competition for food in North America (Koch, 2003). This species has been recently recorded 24
(Klausnitzer, 2004; Majerus et al., 2006). The argentine ant, Linepithema humile (Mayr) is a 1
serious environmental pest in many regions in the world. It has been causing changes in 2
invertebrate and plant communities in the Mediterranean region by predation and 3
displacement of native species (Gómez & Oliveras, 2003). It has been occasionally reported 4
from Switzerland where it reaches its ecological and climatic limit and will probably never 5
cause damage. 6
7
Species comparison between establishment and interception lists
8 9
The most frequently intercepted alien insect species are already established in Europe, if not 10
in the wild, at least in greenhouses and other heated environments, e.g. Bemisia tabaci 11
(Gennadius) (Hem.: Aleyrodidae, 1502 interceptions); Liriomyza huidobrensis (Blanchard) 12
(Dipt.: Agromyzidae, 658); Helicoverpa armigera (Hübner) (Lep.: Noctuidae, 447); 13
Frankliniella occidentalis (Pergande) (Thysan.: Thripidae, 222). However, several other
14
species are very frequently intercepted and are not yet established in Europe, e.g. Tinocallis 15
takachihoensis Higushi (Hem.: Aphidae, 62 records) or Asian Monochamus spp. (Col.:
16
Cerambycidae, 65). On the other hand, many species that are already established in Europe 17
have been very rarely or never intercepted. An interesting case is the recent introduction and 18
spread of the western corn rootworm Diabrotica virgifera virgifera. A recent study showed 19
that the different established populations in Europe originate from different populations 20
(Miller et al., 2005), yet our interception list contains only one record for D. v. virgifera. 21
Altogether, out of the 341 alien insect species in Switzerland and Austria, only 34 (10.0 %) 22
were intercepted by phytosanitary services. On the other hand, only 34 out of the 274 (12.4%) 23
Similarly, only 42 intercepted species are found in the list of 381 (11.0%) alien insects 1
established in the Czech Republic (Šefrová & Laštůvka, 2005). 2
It is not clear why some species are frequently intercepted but never become 3
established, while others are rarely or never intercepted but become established. There are 4
probably numerous factors linked to the species biology and ecology (e.g. climate matching, 5
life cycle, host plant availability, taxonomic isolation of host plants, etc.) or to pathway 6
characteristics (e.g. phytosanitary regulations better implemented for some pathways). It must 7
be noted that more than half of the intercepted species are of tropical or subtropical origin, 8
which decreases the probability of establishment in the wild in most of Europe. 9
Another major constraint to investigate establishment successes is the lack of reliable, 10
rigorous interception data. It may simply be that insects that are established but never 11
intercepted are often introduced but not intercepted on the right pathways at the right moment 12
using the right method. Work et al. (2005) estimated that even rigorous inspections probably 13
detected only 19% to 50% of the imported species, depending on the pathway. In addition, 14
interception surveys focus mainly on quarantine plant pests and targeted commodities (Haack, 15
2006). Insects belonging to economically unimportant groups are not searched for or not 16
identified and only species under quarantine can be stopped entry when founds at ports of 17
entry. Furthermore, non-indigenous insects that are already widely established in Europe are 18
removed from quarantine lists. 19
20
Implications for further studies and management strategies against alien insects
21 22
Evaluation of species traits and habitat characteristics that make insects and habitats 23
prone to invasion is a rewarding step towards understanding insect invasion processes as 24
Lodge, 2001). Such studies, unfortunately, are limited by lack of knowledge of the biology 1
and ecology of most insects, their distribution, especially in natural habitats, and their 2
pathways of introduction. Nevertheless, we were able to determine general patterns 3
characterising invading insects and invaded habitats. For example, our study clearly showed 4
that sap sucking Sternorrhyncha feeding on ornamental plants are more likely to be 5
introduced into a new region than, e.g., Lepidoptera defoliators or Coleoptera root feeders 6
living in natural habitats. However, it is not clear whether such generalizations are of much 7
help in building strategies for the prevention and management of invasive insects. Exceptions 8
are definitively too important to be neglected. For example, the two most damaging alien 9
insects in outdoor agriculture in Europe, the Colorado potato beetle, Leptinotarsa 10
decemlineata (Say), and the western corn rootworm, Diabrotica virgifera virgifera, are both
11
exceptional. Firstly, they are the only alien representatives of the species-rich family 12
Chrysomelidae, which does not seem to include successful invaders in general. Secondly, 13
they belong to two feeding niches, “external defoliators” and “root feeders”, for which we 14
have found relatively few alien species. Thirdly, for neither of these two insects could clear 15
pathway of introduction be identified. Finally, they originate from Mexico and Central 16
America, regions that have not provided many other outdoor-living invaders in Europe. 17
Furthermore, many of the most damaging alien insects are not pests in their region of origin. 18
The two examples cited above were known before their introduction to Europe because they 19
had reached pest status when they invaded the USA and Canada. But other invasive species, 20
such as the horse-chestnut leaf miner Cameraria ohridella, the silver fir woolly aphid 21
Dreyfusia nordmannianae Eckstein and the eastern subterranean termite Reticulitermes
22
flavipes Kollar, were unknown before reaching Europe.
23
These examples unambiguously show that, with invasive alien insects, economic 24
as observed with other taxa (e.g. Levine et al., 2003). The unpredictability of insect 1
introductions and invasiveness, and the fact that the introduction of alien insects is usually 2
accidental and often detected only long after their establishment, put doubts on the usefulness 3
of species-based risk assessments for invasive alien insects (Simberloff, 2005). Standard 4
protocols for species-based risk assessment are most suitable for alien organisms introduced 5
deliberately, and for which an assessment is needed before the probable establishment in the 6
wild, e.g. ornamental plants, fishes, biological control agents, etc. (National Research 7
Council, 2002; Louda et al., 2003) In contrast, strategies against invasive alien insects should 8
focus on specific pathways and awareness building of the relevant authorities (Simberloff et 9
al., 2005). There are few examples of risk assessments for insects aimed at specific pathways.
10
Notable exceptions are the risk assessment procedures developed by US Department of 11
Agriculture to evaluate the risk of importing unprocessed larch from Russia and pine from 12
New Zealand and Mexico (e.g. Tkacz, 2002), but these were also calculated on a species-13
based analysis by combining risks of introducing each particular species that may be 14
transported through these pathways. A better goal would be to define approaches to identify 15
and compare all key pathways and commodities, determine risks associated with each, and 16
sever or restrict the riskiest (Simberloff, 2005). However, until now, too little is known about 17
the pathways of introduction for alien insects to produce risk assessments for key pathways. 18
Interception data in Europe and elsewhere are usually strongly biased according to detection 19
priorities, which depend on pest or commodities of current concern (Haack, 2001, 2006). In 20
addition, there are large discrepancies among countries, ports of entries, etc. Furthermore, 21
insects are not always determined to species level. In the EPPO interception list, 69.8% and 22
88.1% of the insects were determined to species or genus level, respectively, because 23
interception efforts focused mainly on insects of quarantine significance. But in more 24
much lower (e.g. 23% in Work et al., 2005, 35% in Haack, 2006). More importantly, 1
interception data only record positive data, whereas to fully analyse pathways and rates of 2
introduction, negative interceptions also need to be recorded. More studies should focus on 3
specific pathways, using a scientific approach that will produce statistically robust data, such 4
as that of Work et al. (2005). They used statistically-robust data collected by USDA APHIS at 5
US ports of entry as part of the Agricultural Quarantine Inspection Monitoring Protocol 6
(AQUIM, Venette et al., 2002) to estimate arrival rates of non indigenous insects via four 7
cargo pathways: air cargo, refrigerated and non-refrigerated maritime cargo and US-Mexico 8
border cargo. They determined the risks of invasion associated with each of these pathways 9
and were able to evaluate the effectiveness of current efforts to monitor arrival of alien 10
species. We strongly encourage the development of similar investigations on pathways of 11
introduction in Europe. 12
Despite important limits and bias, our analyses of pathways and vectors of 13
introduction were useful in identifying important patterns. In particular, they clearly showed 14
that host plants, especially ornamentals, are the most important vector for the introduction of 15
alien insects into Europe. More than half of the interceptions of alien insects in Europe were 16
made on cut flowers, seedlings, potted plants or bonsai trees. Our results on the most likely 17
pathways for introductions of established insects in Austria and Switzerland also emphasized 18
the role of ornamental plants as vectors. Similarly, Smith et al. (2005) found that all but one 19
of the significant invertebrate plant pests established in Great Britain after 1970 were on 20
ornamentals. Work et al. (2005) showed that 69% of the insect interceptions in air cargos 21
were on cut flowers whereas, in the US-Mexico border cargo, 75% of the insect interceptions 22
were associated with ornamental palms. Interestingly, the ornamental trade is also responsible 23
for the introduction and establishment of the majority of the most serious invasive plants in 24
Europe (Pyšek et al., 2002) and elsewhere (Reichard & White, 2001). Similarly, many of the
most invasive vertebrates in Europe, such as the grey squirrel Sciurus carolinensis and the 1
ruddy duck Oxyura jamaicensis, were initially introduced for aesthetic purposes (Wittenberg, 2
2005). Ornamental plants are by no means essential commodities for human welfare. 3
Therefore, their intercontinental trade should be more regulated. Instead, priority should be 4
given to locally grown indigenous plants. The importance of minor ornamental trades in the 5
introduction of invasive species is exemplified by the trade in bonsai trees. Nearly twice as 6
many pest insects are intercepted on bonsai trees as on timber. Insects intercepted on bonsai 7
trees include many aphids such as Cinara spp., Tinocallis viridis (Takahashi) and T. 8
takachihoensis and scales such as Saissetia neglecta DeLotto, but also long-horned beetles of
9
the genus Anoplophora. The bonsai trade is known to be responsible for the introduction of at 10
least one major tree pest in France, Italy and USA in recent years, the citrus longhorned beetle 11
Anoplophora chinensis (Förster) (Hérard et al., 2005; Haack, 2006).
12
This survey also showed that there is little information on the ecological impact of 13
invasive insects in Europe. In other parts of the world, quite a few invasive insects are known 14
to cause serious damage to the environment, but the impact is most often noticed when 15
“valuable” plant or animal species or entire ecosystems are affected, such as the hemlock and 16
balsam woolly adelgids Adelges tsugae and A. piceae destroying forest ecosystems in North 17
America, or the red fire ant Solenopsis invicta and the Formosan termite Coptotermes 18
formosanus causing structural damages to various ecosystems in Southern USA (Pimentel et
19
al., 2002a). There is a need for studies to properly assess the ecological impact of invasive
20
alien insects and take the appropriate conservation measures. In this paper, we showed that 21
only a minority of the alien insects in Central Europe live in natural habitats and, 22
consequently, have the potential to be detrimental to natural ecosystems. However, it is not 23
clear whether these data reflect a balanced view or just a lack of entomological and ecological 24
1
Acknowledgements 2
3
We would like to thank F. Petter, A.Orlinski and A.S. Roy (EPPO Secretariat, Paris) for 4
access to the EPPO database on plant pest interceptions in Europe, Y. de Jong (Fauna 5
Europaea) for quantitative data on European insects, and M. Cock (CABI Bioscience 6
Switzerland Centre) and two anonymous reviewers for their comments on the manuscript. 7
This work was funded by the EU 6th FWP projects ALARM (GOCE-CT-2003-506675) and 8 DAISIE (SSPI-CT-2003-511202). 9 10 References 11 12
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Figure legends
Fig. 1. Proportional representation of the areas of origin of the 341 non-indigenous insects established in Austria and Switzerland
Fig. 2. Proportional representation of the origin of the commodities on which non-indigenous insects were intercepted by national phytosanitary services in Europe, 1995-2004.
Fig. 3. Proportions of insect orders and sub-orders in the 341 non-indigenous insect species in Austria and Switzerland (black bars) compared to the European insect fauna (source: Fauna Europaea, 2005) (white bars). Orders that were not treated in the Austrian and Swiss lists (e.g. all Apterygote, Mallophaga) were excluded from the analysis. “Others” include small orders (<0.4%) for which no non.-indigenous species are known from Austria and Switzerland, i.e. Dermaptera, Mecoptera, Odonata, Phasmatodea, Strepsiptera.
Fig. 4. Proportions of insect orders and sub-orders in the 341 non-indigenous insect species in Austria and Switzerland originating from North America (black bars) compared to the North American insect fauna (Simberloff, 1986) (white bars). Orders that were not treated in the Swiss and Austrian lists (e.g. all Apterygote, Mallophaga) were excluded from the analysis. “Others” include small orders (<0.4%) for which no non.-indigenous species are known from Switzerland and Austria, i.e. Dermaptera, Mecoptera, Phasmatodea, Strepsiptera.
Fig. 5. Proportion of insect orders and sub-orders in the non-indigenous insects intercepted by national phytosanitary services in Europe, 1995-2004. Black bars indicate the number of interceptions. White bars indicate the number of species intercepted.
Fig. 6. Proportional representation of the feeding niches of the 341 non-indigenous insects in Austria and Switzerland (black bars) and of the European insect fauna (white bars)
Fig. 7. Proportional representation of the environments and host plants of the 341 non-indigenous insects in Austria and Switzerland.
Table 1. A selection of alien insect species recorded in only Switzerland or only Austria.
Recorded only in Switzerland Recorded only in Austria
Aedes albopictus (Skuse) [Dipt. Culicidae] Anoplophora glabripennis (Motschulsky) [Col.: Cerambycidae] Cacyreus marshalli (Butler) [Lep.: Lycaenidae] Antheraea yamamai Guerin-Men. [Lep. Saturniidae]
Corythucha arcuata (Say) [Hem.: Tingidae] Diuraphis noxia (Kurdjumov) [Hem.: Aphidae] Orientus ishidae (Matsumura) [Hem.: Cicadellidae] Lignyodes bischoffi (Blatchley) [Col.: Curculionidae] Pulvinaria regalis Canard [Hem.: Coccidae] Macropsis elaeagni Emeljanov [Hem.: Cicadellidae] Rhagoletis completa Cresson [Dipt. Tephritidae] Phyllonorycter issikii (Kumata) [Lep.: Gracillariidae] Rodolia cardinalis (Mulsant) [Col. : Coccinellidae] Sceliphron caementarium (Drury) [Hym.: Sphecidae]
Table 2: Relative importance of pathways and commodities associated with insect interceptions in Europe during 1995-2004.
Pathway Commodity No. Interceptions %Interceptions
Ornamental trade Aquarium plants 305 4.5
Bonsai trees 281 4.2
Cut Flowers 1939 28.8
Plants for planting 1003 14.9
Seeds 20 0.3
Food products Fruits 753 11.2
Stored products 610 9.0
Vegetables 1343 19.9
Wood and derivates Wood/ Bark 190 2.8
Wood Package 293 4.3
Miscellaneous Unclear 6 0.1
Total 6743 100
Fig. 7.
0 5 10 15 20 25 30 35
Fig. 9.
0 5 10 15 20 25 30 35 40 45 50
Fresh host plant Wood Stored products Host animal Released for biocontrol Escaped Others Multiple/unknown
